J Integr Plant Biol ›› 2025, Vol. 67 ›› Issue (7): 1947-1964.DOI: 10.1111/jipb.13899

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  • 收稿日期:2024-11-13 接受日期:2025-02-27 出版日期:2025-07-01 发布日期:2025-07-07

A SlMYB78-regulated bifunctional gene cluster for phenolamide and salicylic acid biosynthesis during tomato domestication, reducing disease resistance

Peng Cao1,2†, Linghao Xia1,2†, Xianggui Li1,2†, Meng Deng1,2†, Zhonghui Zhang1,2, Xiangyu Lin1,2, Zeyong Wu1,2, Yingchen Hao1,2, Penghui Liu1,2, Chao Wang1,2, Chun Li1,2, Jie Yang1,2, Jun Lai1,2, Jun Yang1,2* and Shouchuang Wang1,2,3*   

  1. 1. National Key Laboratory for Tropical Crop Breeding, School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication), Hainan University, Sanya 572025, China
    2. National Key Laboratory for Tropical Crop Breeding, College of Tropical Agriculture and Forestry, Hainan University, Sanya 572025, China
    3. Yazhouwan National Laboratory, Sanya 572025, China

    †These authors contributed equally to this work.
    *Correspondences: Jun Yang (yang9yj@hainanu.edu.cn); Shouchuang Wang (shouchuang.wang@hainanu.edu.cn, Dr. Wang is fully responsible for the distribution of all materials associated with this article)
  • Received:2024-11-13 Accepted:2025-02-27 Online:2025-07-01 Published:2025-07-07
  • Supported by:
    This work was financially supported by grants from the National Key Research and Development Program of China (2022YFF1001900), the Hainan Province Science and Technology Special Fund (No. ZDYF2022XDNY144), the Hainan Provincial Academician Innovation Platform Project (No. HDYSZX‐202004), the Hainan University Startup Fund (No. KYQD (ZR) 21025), the Collaborative Innovation Center of Nanfan and High‐Efficiency Tropical Agriculture, Hainan University (No. XTCX2022NYB06).

Abstract: Plants have evolved a sophisticated chemical defense network to counteract pathogens, with phenolamides and salicylic acid (SA) playing pivotal roles in the immune response. However, the synergistic regulatory mechanisms of their biosynthesis remain to be explored. Here, we identified a biosynthetic gene cluster on chromosome 2 (BGC2) associated with the biosynthesis of phenolamide and SA, wherein the key component SlEPS1 exhibits dual catalytic functions for the synthesis of phenolamides and SA. Overexpression of the key component SlEPS1 of BGC2 in tomato enhanced resistance to the bacterial pathogen Pst DC3000, whereas knockout plants were more susceptible. Exogenous applications of SA and phenolamides revealed that these two compounds act synergistically to enhance plant resistance. Notably, during tomato domestication, a disease-resistant allele of SlEPS1, SlEPS1HapB, was subject to negative selection, leading to a reduction in phenolamide and SA levels and compromised disease resistance in modern varieties. Moreover, the SlMYB78 directly regulates the BGC2 gene cluster to enhance phenolamide and SA biosynthesis, modulating resistance to Pst DC3000. Our study employed multi-omics approaches to describe the synergistic regulation of phenolamide and SA biosynthesis, offering new insights into the complexity of plant immune-related metabolism.

Key words: bifunctional, disease resistance, domestication, gene cluster, phenolamide, salicylic acid, SlMYB78

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